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Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 1923 Drivers of evolutionary change in Podospora anserina SANDRA LORENA AMENT-VELÁSQUEZ ACTA UNIVERSITATIS UPSALIENSIS ISSN 1651-6214 ISBN 978-91-513-0921-7 UPPSALA urn:nbn:se:uu:diva-407766 2020 Dissertation presented at Uppsala University to be publicly examined in Ekmansalen, Evolutionary Biology Centre (EBC), Norbyvägen 18D, Uppsala, Tuesday, 19 May 2020 at 10:00 for the degree of Doctor of Philosophy (Faculty of Theology). The examination will be conducted in English. Faculty examiner: Professor Bengt Olle Bengtsson (Lund University). Abstract Ament-Velásquez, S. L. 2020. Drivers of evolutionary change in Podospora anserina. Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 1923. 63 pp. Uppsala: Acta Universitatis Upsaliensis. ISBN 978-91-513-0921-7. Genomic diversity is shaped by a myriad of forces acting in different directions. Some genes work in concert with the interests of the organism, often shaped by natural selection, while others follow their own interests. The latter genes are considered “selfish”, behaving either neutrally to the host, or causing it harm. In this thesis, I focused on genes that have substantial fitness effects on the fungus Podospora anserina and relatives, but whose effects are very contrasting. In Papers I and II, I explored the evolution of a particular type of selfish genetic elements that cause meiotic drive. Meiotic drivers manipulate the outcome of meiosis to achieve overrepresentation in the progeny, thus increasing their likelihood of invading and propagating in a population. In P. anserina there are multiple meiotic drivers but their genetic basis was previously unknown. In Paper I, we demonstrated that drive is caused by members of the Spok gene family. We discovered two new Spok genes, Spok3 and Spok4, which locate in different chromosomes in different strains. In Paper II, we showed that Spok3 and Spok4 are found on a gigantic (up to 247 Kb long) variant of Enterprise, a Crypton-like transposable element. Enterprise likely mobilize through the action of a putative tyrosine-recombinase that we call Kirc. When carrying the Spoks, this element has double selfish properties: transposition and meiotic drive. In addition, we found that homologs of the Spoks (Paper I) and of Kirc (Paper II) are widespread in fungi but their phylogenies are discordant with that of the species, suggesting that they have undergone horizontal gene transfer. In Papers III and IV, I turned the focus into genes that have an adaptive function. In fungi, the het genes control conspecific self/ non-self recognition. Such genes are expected to evolve under frequency-dependent balancing selection. In Paper III, we found evidence of balancing selection acting on some het genes across the P. anserina species complex. Unexpectedly, we also discovered that het genes of the HNWD gene family are duplicated in a transposon-like manner, broadening our understanding of their potential fitness effects. Finally, in Paper IV we show how het genes with pleiotropic effects on sexual recognition lead to the evolution of strong reproductive isolation, and hence speciation. Overall, the results of my thesis highlight the functional intersection between mobile selfish genetic elements and other genes, either selfish or adaptive, and their effects on genome architecture and population structure. Keywords: Podospora, Meiotic drive, Spore killing, vegetative incompatibility, heterokaryon incompatibility, allorecognition, speciation, Transposable elements, selfish genetic elements, fungi Sandra Lorena Ament-Velásquez, Department of Organismal Biology, Systematic Biology, Norbyv. 18 D, Uppsala University, SE-75236 Uppsala, Sweden. © Sandra Lorena Ament-Velásquez 2020 ISSN 1651-6214 ISBN 978-91-513-0921-7 urn:nbn:se:uu:diva-407766 (http://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-407766) A mis padres List of Papers This thesis is based on the following papers, which are referred to in the text by their Roman numerals. I Vogan, A.A.*, Ament-Velásquez, S.L.*, Granger-Farbos, A., Sved- berg, J., Bastiaans, E., Debets, A.J., Coustou, V., Yvanne, H., Clavé, C., Saupe, S.J., Johannesson, H. (2019) Combinations of Spok genes create multiple meiotic drivers in Podospora. eLife, 8: e46454 II Vogan, A.A., Ament-Velásquez, S.L., Bastiaans, E., Wallerman, O., Saupe, S.J., Suh, A., Johannesson, H. (-) The Enterprise: A mas- sive transposon carrying Spok meiotic drive genes. Manuscript III Ament-Velásquez, S.L., Vogan, A.A., Wallerman, O., Hartmann, F., Gautier, V., Silar, P., Giraud, T., Johannesson, H. (-) The evolu- tion of the allorecognition gene repertoire in the Podospora species complex. Manuscript IV Ament-Velásquez, S.L., Vogan, A.A., Granger-Farbos, A., Bas- tiaans, E., Martinossi-Allibert, I., Saupe, S.J., de Groot, S., Lascoux, M., Debets, A.J.M., Clavé, C., Johannesson, H. (-) Allorecognition genes drive reproductive isolation in Podospora anserina. Manu- script Reprints were made with permission from the respective publishers. * These authors contributed equally Additional papers The following papers were published during the course of my doctoral stud- ies, but are not part of this thesis. Ament-Velásquez, S.L., Breedy, O., Cortés, J., Guzman, H.M.H.M., Wörheide, G., Vargas, S., (2016). Homoplasious colony morphology and mito-nuclear phylogenetic discordance among Eastern Pacific Octocorals. Molecular Phylogenetics and Evolution, 98: 373–81 Ament-Velásquez, S.L., Figuet, E., Ballenghien, M., Zattara, E.E., Noren- burg, J.L., Fernández-Álvarez, F.A., Bierne, J., Bierne, N., Galtier, N. (2016). Population genomics of sexual and asexual lineages in fissiparous ribbon worms (Lineus, Nemertea): Hybridization, polyploidy and the Me- selson Effect. Molecular Ecology, 25 (14): 3356–69 Contents Introduction ................................................................................................... 11 Intragenomic conflict and meiotic drive as evolutionary forces .............. 12 An observable case of meiotic drive: spore killing in fungi ..................... 17 Examples of spore killers ..................................................................... 18 The protagonists: Podospora anserina and allied taxa ............................ 20 A peculiar life cycle ............................................................................. 22 Reproductive biology of fungi and of P. anserina .............................. 22 To fuse or not to fuse: the heterokaryon incompatibility system ............. 26 NLRs: a recurrent theme in the structure of intracellular guardians .... 29 Research aims ................................................................................................ 32 Summary of results ....................................................................................... 33 The genetic basis and evolution of meiotic drive in Podospora anserina (Papers I and II) ........................................................................................ 33 The intersection between allorecognition genes and other recognition systems in Podospora (Papers III and IV) ................................................ 35 Conclusions and future prospects .................................................................. 38 Svensk sammanfattning ................................................................................. 41 Resumen en español ...................................................................................... 43 Acknowledgments ......................................................................................... 45 Cover explanation ......................................................................................... 54 References ..................................................................................................... 55 Abbreviations DNA Deoxyribonucleic acid bp, kb, Mb Base pair, Kilo base, Mega base het Heterokaryon incompatibility gene Indel Insertion / Deletion TE Transposable element LTR Long terminal region LD Linkage disequilibrium PCR Polymerase chain reaction SNP Single nucleotide polymorphism VI Vegetative incompatibility reaction π Nucleotide diversity θw Watterson’s theta Dxy Average number of pairwise differences Introduction In a report meant to introduce the filamentous fungus Podospora anserina (Ces. Ex Rabenh.) Niessl as a model organism, the German geneticist Karl Esser wrote “The reader may ask, why are these Europeans using such a strange and, from the first glance, rather complicated organism as Podo- spora, and, why do they not integrate into the large family of Neurosporolo- gists?” (Esser, 1969). To answer, he then proceeded to list a number of rea- sons as to why P. anserina is great for research. They included things that are important in model organisms, like a short life cycle and the amenability to mutagenesis, but also other properties like the easy isolation of haploid spores, no asexual propagules to contaminate other plates, and interesting biological aspects of its life cycle. With my work, I wish to add to this list by emphasizing the use of P. anserina as a model organism for the study of fundamental questions in evolution biology. In tune with traditional Podospora literature, the focus of my research is heavily gene-centric. Specifically, I gravitate around two types of genes: selfish and allorecognition genes. Selfish genetic elements (including pro- tein-coding genes) are parasitic units
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  • The Genus Podospora (Lasiosphaeriaceae, Sordariales) in Brazil

    The Genus Podospora (Lasiosphaeriaceae, Sordariales) in Brazil

    Mycosphere 6 (2): 201–215(2015) ISSN 2077 7019 www.mycosphere.org Article Mycosphere Copyright © 2015 Online Edition Doi 10.5943/mycosphere/6/2/10 The genus Podospora (Lasiosphaeriaceae, Sordariales) in Brazil Melo RFR1, Miller AN2 and Maia LC1 1Universidade Federal de Pernambuco, Departamento de Micologia, Centro de Ciências Biológicas, Avenida da Engenharia, s/n, 50740–600, Recife, Pernambuco, Brazil. [email protected] 2 Illinois Natural History Survey, University of Illinois, 1816 S. Oak St., Champaign, IL 61820 Melo RFR, Miller AN, MAIA LC 2015 – The genus Podospora (Lasiosphaeriaceae, Sordariales) in Brazil. Mycosphere 6(2), 201–215, Doi 10.5943/mycosphere/6/2/10 Abstract Coprophilous species of Podospora reported from Brazil are discussed. Thirteen species are recorded for the first time in Northeastern Brazil (Pernambuco) on herbivore dung. Podospora appendiculata, P. australis, P. decipiens, P. globosa and P. pleiospora are reported for the first time in Brazil, while P. ostlingospora and P. prethopodalis are reported for the first time from South America. Descriptions, figures and a comparative table are provided, along with an identification key to all known species of the genus in Brazil. Key words – Ascomycota – coprophilous fungi – taxonomy Introduction Podospora Ces. is one of the most common coprophilous ascomycetes genera worldwide, rarely absent in any survey of fungi on herbivore dung (Doveri, 2008). It is characterized by dark coloured, non-stromatic perithecia, with coriaceous or pseudobombardioid peridium, vestiture varying from glabrous to tomentose, unitunicate, non-amyloid, 4- to multispored asci usually lacking an apical ring and transversely uniseptate two-celled ascospores, delimitating a head cell and a hyaline pedicel, frequently equipped with distinctly shaped gelatinous caudae (Lundqvist, 1972).